Metabolic symbiosis at the origin of eukaryotes.

Thirty years after Margulis revived the endosymbiosis theory for the origin of mitochondria and chloroplasts, two novel symbiosis hypotheses for the origin of eukaryotes have been put forward. Both propose that eukaryotes arose through metabolic symbiosis (syntrophy) between eubacteria and methanogenic Archaea. They also propose that this was mediated by interspecies hydrogen transfer and that, initially, mitochondria were anaerobic. These hypotheses explain the mosaic character of eukaryotes (i.e. an archaeal-like genetic machinery and a eubacterial-like metabolism), as well as distinct eukaryotic characteristics (which are proposed to be products of symbiosis). Combined data from comparative genomics, microbial ecology and the fossil record should help to test their validity.

[1]  G. B. Golding,et al.  The mosaic nature of the eukaryotic nucleus. , 1998, Molecular biology and evolution.

[2]  M W Gray,et al.  The evolutionary origins of organelles. , 1989, Trends in genetics : TIG.

[3]  M. Sogin.  Early evolution and the origin of eukaryotes , 1991, Current Biology.

[4]  B. Runnegar,et al.  Megascopic eukaryotic algae from the 2.1-billion-year-old negaunee iron-formation, Michigan. , 1992, Science.

[5]  P. Albrecht,et al.  Polar Lipids of Archaebacteria in Sediments and Petroleums , 1982, Science.

[6]  Eörs Szathmáry,et al.  The Major Transitions in Evolution , 1997 .

[7]  J. Cole,et al.  Isolation and characterization of a novel bacterium growing via reductive dehalogenation of 2-chlorophenol , 1994, Applied and environmental microbiology.

[8]  T. Sicheritz-Pontén,et al.  The genome sequence of Rickettsia prowazekii and the origin of mitochondria , 1998, Nature.

[9]  Purificación López-García,et al.  Symbiosis Between Methanogenic Archaea and δ-Proteobacteria as the Origin of Eukaryotes: The Syntrophic Hypothesis , 1998, Journal of Molecular Evolution.

[10]  M. Henk,et al.  Filamentous sulfide‐oxidizing bacteria at hydrocarbon seeps of the Gulf of Mexico , 1996, Microscopy research and technique.

[11]  D. Karl,et al.  Phylogenetic diversity of the bacterial community from a microbial mat at an active, hydrothermal vent system, Loihi Seamount, Hawaii , 1995, Applied and environmental microbiology.

[12]  J. Felsenstein.  Cases in which Parsimony or Compatibility Methods will be Positively Misleading , 1978 .

[13]  M. Dworkin.  Recent advances in the social and developmental biology of the myxobacteria. , 1996, Microbiological reviews.

[14]  C. Woese,et al.  Phylogenetic structure of the prokaryotic domain: The primary kingdoms , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[15]  W. Doolittle,et al.  Cytoskeletal proteins: The evolution of cell division , 1998, Current Biology.

[16]  W. Doolittle,et al.  Tempo, mode, the progenote, and the universal root. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[17]  G. B. Golding,et al.  The origin of the eukaryotic cell. , 1996, Trends in biochemical sciences.

[18]  O. Kandler,et al.  Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[19]  W. Zillig.  Comparative biochemistry of Archaea and Bacteria. , 1991, Current opinion in genetics & development.

[20]  R. Summons,et al.  Hydrocarbon shows and petroleum source rocks in sediments as old as 1.7 × 109 years , 1986, Nature.

[21]  W. Martin,et al.  The hydrogen hypothesis for the first eukaryote , 1998, Nature.

[22]  Tibor Vellai,et al.  A New Aspect to the Origin and Evolution of Eukaryotes , 1998, Journal of Molecular Evolution.

[23]  Betsey Dexter Dyer,et al.  The origin of eukaryotic cells , 1985 .

[24]  W. Doolittle.  You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. , 1998, Trends in genetics : TIG.

[25]  L. Margulis.  Symbiosis in cell evolution: Life and its environment on the early earth , 1981 .

[26]  J. Lake,et al.  Genomic evidence for two functionally distinct gene classes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  P. Raven,et al.  ORIGIN OF EUKARYOTIC CELLS , 1971 .

[28]  T. Swain,et al.  Symbiosis in Cell Evolution: by L. Margulis. W. H. Freeman, San Francisco, 1981. xix + 419 pp. , 1983 .

[29]  J. Reeve,et al.  Archaeal DNA binding proteins and chromosome structure , 1993 .

[30]  S. Bengtson.  Early life on earth , 1994 .

[31]  Bland J. Finlay,et al.  Ecology and evolution in anoxic worlds , 1995 .

[32]  M. Lilley,et al.  The quantum event of oceanic crustal accretion: impacts of diking at mid-ocean ridges. , 1998, Science.

[33]  H. Ohmoto,et al.  Bacterial activity in the warmer, sulphate-bearing, Archaean oceans , 1987, Nature.

[34]  J A Lake,et al.  Was the nucleus the first endosymbiont? , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. Lidstrom,et al.  C1 transfer enzymes and coenzymes linking methylotrophic bacteria and methanogenic Archaea. , 1998, Science.